(2015), 40(1): pp. 269–285 Date of publication February 12 ...€¦ · SMZ1500 stereomicroscope...

Systematic Botany (2015), 40(1): pp. 269–285© Copyright 2015 by the American Society of Plant TaxonomistsDOI 10.1600/036364415X686567Date of publication February 12, 2015

A Phylogenetically Based Infrageneric Classification of the ParasiticPlant Genus Cuscuta (Dodders, Convolvulaceae)

Mihai Costea,1,3 Miguel A. Garcıa,2 and Sasa Stefanovic2

1Department of Biology, Wilfrid Laurier University, Waterloo, Ontario N2L3C5, Canada.2Department of Biology, University of Toronto Mississauga, Mississauga, Ontario L5L 1C6, Canada.

3Author for correspondence ([email protected])

Communicating Editor: Jennifer A. Tate

Abstract—Cuscuta (dodders, Convolvulaceae) is one of the largest and most economically important lineages of parasitic plants. The genushas a sub-cosmopolitan distribution with more than 75% of the species diversifying in the New World. The last monograph, published byTruman George Yuncker in 1932, provided a solid species-level taxonomic foundation. However, as revealed by recent phylogenetic studies,its infrageneric classification has been in great need of a taxonomic reappraisal, mainly because the morphological characters used in theprevious classifications have been greatly affected by convergent evolution. Several recent phylogenetic and character evolution studies withbroad sampling, as well as species-level revisions, have illustrated the deficiencies of previous classifications and provided an explicit androbust phylogenetic framework. Here we propose a new phylogenetic classification that places all 194 currently accepted species of Cuscutainto four subgenera and 18 sections. Sections have a strong morphological and biogeographical predictive value and include from one to31 species. Thirteen section names are new or applied for the first time at the sectional rank: Babylonicae (Yunck.) M. A. Garcıa, Subulatae(Engelm.) Costea & Stefanovic,Obtusilobae (Engelm.) Costea & Stefanovic, Prismaticae (Yunck.) Costea & Stefanovic, Ceratophorae (Yunck.)Costea & Stefanovic, Umbellatae (Yunck.) Costea & Stefanovic, Gracillimae Costea & Stefanovic, Californicae (Yunck.) Costea & Stefanovic,Indecorae (Yunck.) Costea & Stefanovic, Oxycarpae (Engelm. ex Yunck.) Costea & Stefanovic, Racemosae (Yunck.) Costea & Stefanovic,Partitae Costea & Stefanovic, and Denticulatae (Yunck.) Costea & Stefanovic. An identification key to sections is included together with anoverview of morphology, geographical distribution, taxonomic notes, and lists of included species.

Keywords—Molecular phylogeny, morphology, systematics, taxonomy.

Cuscuta (dodder) is a genus of nearly 200 species of stemparasites that has evolved within Convolvulaceae (reviewedby Stefanovic and Olmstead 2004, 2005). Dodder embryoslack cotyledons; their radicle is devoid of apical meristemsand degenerates a few days after germination (Truscott 1966;Sherman et al. 2008). Another distinctive characteristic of thisparasitic lineage is the diversity of photosynthetic capabilitiesand plastome reductions at clade and at species levels, whichaccompanied transitions from hetero- to holoparasitism(reviewed by Braukmann et al. 2013). The genus is nearlycosmopolitan, but the majority of species (ca. 75%) are nativeto North and South America. Dodders occur in a great varietyof habitats, from temperate to tropical, desert to riparian, litto-ral to high mountains, grasslands, forests, saline, and dis-turbed habitats. Similarly to other parasitic plants, doddersact as keystone species in their ecosystems (Press and Phoenix2005). Approximately 15–20 Cuscuta sp. worldwide are agri-cultural and horticultural pests (Dawson et al. 1994; Costeaand Tardif 2006), and in most countries the control and quar-antine measures target the genus as a whole, ignoring the factthat more species may be endangered or even threatened withextinction (Costea and Stefanovic 2009a).Remarks about the peculiar morphology of Cuscuta and its

parasitic nature date back to the Babylonian Talmud andDioscorides, while the etymology of the generic name can beretraced to Aramaic and/or ancient Hebrew (Costea andTardif 2004). As a distinct group, Cuscuta had been recog-nized before Linnaeus by Bauhin (1623), Ray (1682), andTournefort (1694). In 1753, Linnaean Cuscuta included onlytwo species: C. europaea (including C. europaea var. epithymum)and C. americana (Linnaeus 1753). Choisy (1841) published thefirst monograph of Cuscuta, in which he increased the numberof known species to 38 and provided the first infragenericclassification based on the shape of stigmas. His “Sectio prima”with acute/clavate stigmas and “Sectio secunda” with globose-capitate stigmas circumscribe the major infrageneric groupsknown today as subgenera Cuscuta and Grammica, respec-

tively. The next monograph of the genus was provided byEngelmann (1859), who added 57 new species and used styleand stigma characters to delimit three major (unranked)“Groups” of dodders: Cuscuta, with two styles and elongatedstigmas; Grammica with two styles and capitate stigmas; andMonogynella with one style and variously shaped stigmas.Subsequent botanists and scholars of Cuscuta (e.g. Peter 1891;Mirande 1900; Yuncker 1921, 1932, 1965; Hunziker 1949, 1950)endorsed this delimitation with three subgenera, which havebeen universally accepted until today. In contrast to the defi-nition of subgenera, the separation of infrageneric taxa belowthe rank of subgenus has varied considerably from author toauthor. Engelmann (1859) defined nine sections and six sub-sections. Yuncker (1932) proposed an intricate infragenericclassification with eight sections and 32 subsections. Finally,Hunziker, in treatments of Cuscuta from Argentina andUruguay (Hunziker 1949, 1950), added two new subsectionsto Yuncker’s classification of subgenus Grammica.During the last decade, our understanding of Cuscuta sys-

tematics has been substantially enhanced bymolecular studiesaimed at unraveling evolutionary relationships at differenttaxonomic levels, character evolution, and biogeography.Two broad-level molecular phylogenetic studies based onplastid (pt) trnL-UAA/trnF-GAA and nuclear ribosomal (nr)ITS sequences tested the monophyly of subgenera Cuscuta andGrammica and provided the relationships among their majorinfrageneric clades (Garcıa and Martın 2007; Stefanovic et al.2007). Similar results were also obtained in a study by McNealet al. (2007), which was less comprehensive in terms of taxonsampling but included representatives from across the entiregenus as well as additional pt sequences (rps2 and matK).Finally, in the most comprehensive phylogenetic study to datewe expanded our previous sampling and existing matrices tothe entire genus using coding plastid and nuclear sequencedata (rbcL and nrLSU, respectively) from a wide taxonomicsampling and covering its morphological, physiological, andgeographical diversity (Garcıa et al. 2014). While these recent

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studies have largely confirmed the three major groups/subgenera proposed by Engelmann, the delimitation of a fourthmajor lineage, “Pachystigma”, which includes South Africanspecies, emerged as a necessity. Subgenus Cuscuta was foundto be paraphyletic, with the South African members of thissubgenus (sect. Pachystigma) more closely related to subgenusGrammica, as previously suggested by McNeal et al. (2007)based on a limited sampling. In addition, much more substan-tial changes were revealed at a sectional level, particularly inthe largest infrageneric group, subgenus Grammica (153 spe-cies; ~3/4 of species diversity of the genus). In contrast toYuncker’s classification of subg. Grammica with 2 sections and24 subsections, our results have indicated the existence of15 well-supported major clades (labeled informally A–O inStefanovic et al. 2007, Stefanovic and Costea 2008; Garcıa et al.2014). Moreover, the species make-up of these groups divergessignificantly from the taxonomic arrangements of Engelmann(1859) and Yuncker (1932). Also, a series of focused studiesexplored in depth the species-level evolutionary relationshipswithin nine of the 15 majorGrammica clades (Costea et al. 2005,2006a, b, c, 2008a, 2009, 2011a, b, 2013; Costea and Stefanovic2009b, 2010). All of these studies emphasized the necessity fora new infrageneric classification and nomenclatural schemefor Cuscuta. Thus the main objective of this study is to incor-porate all of the above mentioned phylogenetic results into anew formal infrageneric classification of this genus, in conjunc-tion with a re-evaluation of traditional taxonomic characters.

Materials and Methods

This infrageneric classification is based on the molecular phylogeneticframework provided primarily by the studies of Garcıa and Martın (2007),Stefanovic et al. (2007), and Garcıa et al. (2014). The infrageneric taxaproposed, four subgenera and 18 sections, are all monophyletic (Fig. 1).The smallest section is monotypic and the largest includes 31 species. Tomaximize nomenclatural stability, whenever possible, we retained theavailable infrageneric names, although especially in subg. Grammica mostof these names are applied for the first time at the sectional rank. For thispurpose, all the previous infrageneric names were typified. In the case ofRafinesque’s generic names, the problem is not strictly typification,because at least one species was indicated by the author for each genus(Rafinesque 1836), but rather determining the identity of these Cuscutaspecies. Yuncker (1921, 1932) and Manitz (1976) elucidated the identity ofmost of these species names, and we proposed Cuscuta synonyms for theremaining ones.Three hybrid species, each involving parents from two different clades

of subgenus Grammica, C. sandwichiana, C. bifurcata, and C. xanthochortos(Stefanovic and Costea 2008; Garcıa et al. 2014), were assigned to one oftheir respective “progenitor” clades based on their morphological affini-ties. The classification included all the accepted species even if some ofthem could not be studied in previous molecular studies. The latter spe-cies are often known only from the type specimen(s), and a provisionalplacement was proposed based on their morphology. These species areindicated with an asterisk (“*”) in the “included species” of each section.A few remaining species with an uncertain status were also consideredand their placement discussed separately. Thus, this study also repre-sents the most accurate species count of genus Cuscuta to date.

Cuscuta collections from the following herbaria were studied andannotated: AAU, ABH, ALTA, ARAN, ARIZ, ASU, B, BAB, BC, BCN,BM, BOL, BORD, BR, BRIT, CAL, CANB, CAS, CEN, CHR, CHSC,CIIDIR, CIMI, COI, CTES, DAO, E, F, FT, G, GH, H, HUFU, HUJ, IAC,IEB, IND, J, JACA, JE, JEPS, K, L, LAU, LD, LE, LL, LP, LPB, LPS, M, MA,MACB, MAF, MEL, MERL, MEXU, MGC, MICH, MO, MPU, MSTR,NAP, NBG, NMC, NY, OAC, OKLA, OSC, OXF, P, PACA, PRE, QCNE,QFA, RB, RNG, RSA, S, SALA, SAM, SASK, SD, SEV, SGO, SI, SPF, TEX,TRT, TRTE, UA, UB, UBC, UCR, UCT, UNB, UNM, UPRRP, UPS, US,VAL, W, WTU, and XAL.Morphological characters used to define subgenera and sections are

based on Engelmann (1859), Yuncker (1932, 1965), a series of recent spe-cies-level systematic studies (see introduction), and several character evo-

lution studies of the pollen, perianth, infrastaminal scales, andgynoecium in Cuscuta (Welsh et al. 2010; Wright et al. 2011, 2012; Riviereet al. 2013; Garcıa et al. 2014). Morphological characteristics of subgeneraand sections are shown in Figs. 2, 3, 4. Stereomicroscopy images weretaken from rehydrated flowers of herbarium specimens using a NikonSMZ1500 stereomicroscope equipped with a PaxCam Arc digital cameraand Pax-it 7.5 software (MIS Inc., Villa Park, Illinois, released 2014). Forscanning electron microscopy (SEM), we used hexamethydisilazane(HMDS) as an alternative for critical point drying (Costea et al. 2011a, b).Examination, measurements and pictures were taken at 10 kV using aHitachi SU1510 variable pressure scanning electron microscope. Thou-sands of photographs that illustrate details of the floral parts, pollen, andfruit morphology are available on the Digital Atlas of Cuscuta (Costea2007-onwards).

Discussion

Convergent Evolution Hindered Previous Section-levelClassifications in Cuscuta—Similarly to other parasiticplants (Kuijt 1969), evolution to parasitism in Cuscuta wasaccompanied by a drastic reduction of the vegetative organs(e.g. stems and leaves) and a diversification of the floral partsand breeding systems (Wright et al. 2011, 2012). Therefore,previous classifications of Cuscuta (e.g. Engelmann 1859;Yuncker 1932) had to rely entirely on flower and fruit charac-teristics. However, recent systematic investigations at thespecies level (see introduction) and character evolution stud-ies revealed that the majority of morphological characters inCuscuta are significantly affected by convergent evolution.Such characters include: perianth features (Wright et al.2012); shape, size, and reduction of infrastaminal scales(Riviere et al. 2013); pollen morphology (Welsh et al. 2010);shape/size of gynoecium/capsule parts (Wright et al. 2011;Garcıa et al. 2014); and fruit dehiscence/indehiscence (Garcıaet al. 2014). For example, Yuncker (1932) considered fruitdehiscence/indehiscence to be of paramount significanceand hypothesized that dehiscent capsules have evolvedfrom indehiscent ones. Accordingly, he divided subgenusGrammica into two sections: Eugrammica with dehiscent cap-sules, and Cleistogrammica with indehiscent capsules. In con-trast, we found that capsule dehiscence is the plesiomorphiccondition while the apomorphic indehiscence has evolvedmultiple times, sometimes with reversals to dehiscence(Garcıa et al. 2014). Thus convergent evolution has obscuredthe natural infrageneric groups, particularly at the sectionlevel and in the species-rich subgenus Grammica, and as aresult, neither the two subsections nor the 24 subsectionsproposed by Yuncker (1932) for the latter subgenus aremonophyletic (Fig. 1).In some cases, entire clades/sections of subg. Grammica

from different continents converge morphologically, in others,only certain species belonging to different clades sharestrong morphological affinities. Convergent evolution withinthe largest clades/sections also took place. For example,Lobostigmae and Subulatae are the largest infrageneric groupsof subg. Grammica (18 and 31 species, respectively); theformer group is North American and the latter SouthAmerican, but both clades have in common large, fleshyflowers, thick styles, and large or lobed stigmas. Thesefloral characteristics likely evolved in association with thetendency towards xenogamy observed in most species ofthese two clades (Wright et al. 2012). Similarly, sect. Oxycarpaefrom North America and Racemosae from South America aredifficult to separate morphologically, and their species havecomparable mixed-mating breeding systems in common(Wright et al. 2012).

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Isolated species from different clades that share strongmorphological affinities are relatively rare; for instance,C. yucatana (sect. Grammica, Mexico; Costea et al. 2011b) andC. acuta (sect. Umbellatae, S America; Costea and Stefanovic2010), and C. carnosa (sect. Ceratophorae, Mexico; Costea et al.2011a) and species from the C. volcanica subclade (sect.Subulatae, Mexico; Costea et al. 2013). Unfortunately, in allthese cases, too little is known about the ecology and the hostrange of the species to attempt a biological explanation oftheir convergent evolution. Alternatively, the morphologicalsimilarity between species from different clades may be theresult of undiscovered reticulate evolution involving speciesfrom both clades, a phenomenon that has been recently doc-

umented in subg. Grammica (Stefanovic and Costea 2008;Costea and Stefanovic 2010; Garcıa et al. 2014).Convergent evolution within the same clade/section did

not affect previous classifications but occasionally it concealedthe existence of some species or it caused species delimitationproblems. For instance, C. montana, recently described fromDurango, Mexico, resembles morphologically C. rugosiceps,but both species belong to different subclades of sect.Lobostigmae (Costea et al. 2013 and the other spp. examplesillustrated there). Similar situations can be also encounteredin other large sections of subg. Grammica (e.g. Subulatae andUmbellatae). An important point, however, is that 90% of thespecies described in the past, often from type specimens only

Fig. 1. The summary evolutionary hypothesis for Cuscuta (dodders; Convolvulaceae) derived from sequence data from plastid (trnL-F, rbcL) andnuclear (nrITS, nrLSU) sources and analyzed with a range of analytical methods (Garcıa and Martın 2007; Stefanovic et al. 2007; Garcıa et al. 2014).Numbers above branches indicate bootstrap support for labeled clades and backbone relationships as reported by Garcıa et al. (2014). Infragenericclassification (subgenera and sections) proposed in this paper is indicated on the left. Numbers in brackets correspond to the number of species found inthose groups (see Taxonomic Treatment). Traditional definitions of sections and subsections following Yuncker (1932; amended in 1965) and theirrelationship with phylogenetic classification are indicated on the right; the number of species assigned within a group by Yuncker is providedin parentheses.

2015] COSTEA ET AL.: PHYLOGENETIC CLASSIFICATION OF CUSCUTA 271

(e.g. by Engelmann, Yuncker, Hunziker), have been vali-dated by modern studies; therefore, morphology is a strongpredictor of species lineages within each section.In conclusion, because of convergent evolution it was

unavoidable that some morphological overlap would occuramong the sections of subgenus Grammica. Even so, the mor-phological predictive value of these new infrageneric groupsis high, in addition to the molecular, biogeographical, andprobably biochemical characters.Cuscuta: One Versus Several Genera—Even though a sin-

gle genus concept has dominated botanical literature, histor-ically Cuscuta was also considered to consist of severaldistinct genera. For example, Loureiro (1790) describedgenus Grammica. Rafinesque (1836) thought that Cuscutaincluded “at least” 10 other genera, which he defined basedon characters that are currently considered appropriate at thespecies level (Cuscuta s. s., Anthanema, Aplostylis, Dactylepis,Eronema, Kadula, Kadurias, Lepimenes, Nemepis, and Pentake).The definition of a monotypic family Cuscutaceae byDumortier (1829) further stimulated the description of newgenera. Note that the different classifications of Cuscuta, eitheras multiple genera of Cuscutaceae or as groups/subgenera ofa unified genus (with the exception of Rafinesque 1836), havealways been based on various interpretations of the morphol-ogy of styles and stigmas (Wright et al. 2011). For example,Pfeiffer (1845) treated Cuscuta as a family with three genera:

Cuscuta with linear stigmas, Epilinella with clavate stigmas,and Engelmannia with capitate stigmas. Des Moulins (1853)segregated the family into five genera: Cuscuta (stigma fili-form), Epilinella (stigma claviform),Monogynella (styles fused),Cassutha [J. Bauh.] (stigma capitate), and Succuta (stigma fili-form). Most recently, Hadac and Chrtek (1970) proposed aclassification with four genera: Cuscuta s. s., Grammica,Monogynella, and Kadurias, and published in this and subse-quent articles a great number of nomenclatural combina-tions: 119 in Grammica, 25 inMonogynella, and five in Kadurias(IPNI 2014). Since none of these multi-generic nomenclaturalinnovations were accompanied by systematic studies, theywere in general not accepted. The characters used, with theexception of the historical gynoecium characters, vary consid-erably across the genus (e.g. the number of chromosomes andnumber of coils in the embryo). More recent character evolu-tion studies have found that Monogynella, the sister group tothe rest of Cuscuta, is quite distinct morphologically comparedto other lineages, Pachystigma, Cuscuta, and Grammica (e.g.Wright et al. 2011; Riviere et al. 2013). However, a mono-generic concept of Cuscuta is backed up by its consistentand strongly supported monophyly within Convolvulaceae(Stefanovic and Olmstead 2004). This approach is also practi-cal, considering the minute morphological differences betweenthe major groups of Cuscuta, which are treated as subgenera inthis article.

Fig. 2. Morphological characteristics of Cuscuta subgenera. A–B. Subgenus Monogynella, one style gynoecium. A. C. japonica. B. C. exaltata, styledistally bifid. C. Subgenus Cuscuta, gynoecium with two equal styles having a ± similar diameter as the cylindrical stigmas, C. epithymum. D. SubgenusPachystigma, gynoecium with two equal or unequal styles, thinner than the clavate stigmas, C. angulata. E. Subgenus Grammica, gynoecium with twounequal styles and capitate stigmas, C. gronovii. F–H. Infrastaminal scales (IFS). F. General position in the flower, C. argentinana. G. IFS fimbriae insubgenus Monogynella, C. reflexa. H. IFS fimbriae in subgenera Cuscuta, Pachystigma, and Grammica, C. campestris. Arrows indicate laticifers (the smoothcells). Scale bars. A–F = 1 mm; G–H = 50 mm.


Fig. 3. Examples of morphological characteristics of Cuscuta sections. A–C. Sect. Cuscuta. A. inflorescence, C. approximata subsp. macranthera.B. Flower, C. epithymum subsp. kotschyi. C. gynoecium, C. epithymum subsp. epithymum. D. Sect. Epistigma, gynoecium, C. kotschyana. E. Sect. Babylonicae,inflorescence, C. babylonica. F. Subg. Pachystigma, inflorescence, C. africana. G–H. Sect. Grammica. G. Flower, C. alata. H. Dissected calyx, C. chinensissubsp. chinensis. I–L. Sect. Subulatae. I. Inflorescence/flowers, C. purpurata. J. Dissected calyx, C. foetida. K. Papillate infrastaminal scale fimbriae,C. rubella. L. Gynoecium, C. odorata. M–N. Sect. Obtusilobae. M. flower, C. americana. N. Dissected calyx, C. americana. O. Sect. Prismaticae, flower,C. prismatica. P–S. Sect. Ceratophorae. P. Flowers, C. boldinghii. R. Gynoecium, C. boldinghii. S. Dissected corolla, C. boldinghii. T–U. Sect. Umbellatae.T. Inflorescence fragment, C. umbellata. U. Capsule, C. umbellata. Scale bars = 1 mm.


Fig. 4. Examples of morphological characteristics of Cuscuta sections. A–C. Sect. Gracillimae. A. Inflorescence, C. gracillima. B. Flowers, C. gracillima.C. Dissected calyx, C. gracillima. D–G. Sect. Cleistogrammica. D. Flower, C. obtusiflora. E. Dissected calyx, C. obtusiflora. F. Dissected corolla, C. campestris.G. Capsule, C. campestris. H–I. Sect. Californicae. H. Flowers, C. californica. I. Dissected corolla, C. californica. J–K. Sect. Indecorae. J. Flower, C. indecora var.indecora. K. Dissected calyx, C. indecora. L–M. Sect. Oxycarpae. L. Flower, C. gronovii var. gronovii. M. Capsule, C. gronovii var. gronovii. N–O. Sect.Racemosae. N. Flower, C. racemosa. O. Capsule, C. racemosa. P–R. Sect. Partitae. P. Flower, C. burrellii. R. Dissected calyx, C. burrellii. S–T. Sect. Denticulatae.S. Dissected calyx, C. denticulata. T. Embryo, C. denticulata; U–W. Sect. Lobostigmae; U, ‘typical’ Cuscuta embryo included as a comparison for sect.Denticulatae, C. woodsonii. V. Flower, C. tasmanica. W. Gynoecium, C. tasmanica. Scale bars = 1 mm.


How Many Species of Cuscuta are Known to Exist?—Yuncker (1932) included 158 species in his monograph. Subse-quent overview works commonly mentioned “about 150” spe-cies even if more species were described after 1932 (e.g. manyincluded in Hunziker 1949, 1950; Yuncker 1965). It is unclearwhy GBIF (2014), EOL (2014), and the many sources followingthem, report a vague 100–170 number of species for this genus.Similarly, The Plant List (2014) included 127 Cuscuta species

with “medium confidence” and 77 with “low confidence” (noteven a single binomial has “high confidence” according to thissource). This level of uncertainty is unacceptable in the case ofCuscuta, which unlike other genera has received a lot of atten-tion from a systematic point of view, both past and present. Toeliminate any ambiguity, we emphasize that we accepted 194species, with more likely to be discovered in the future. In orderto be useful, biodiversity lists must be based on systematics.

Taxonomic Treatment

Key to the Subgenera of CUSCUTA

1. Gynoecium with 1 style, sometimes distally bifid; fimbriae of infrastaminal scales are glandular trichomeswith the secretory cells completely exposed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . I. Subg.Monogynella

1. Gynoecium with 2 styles; fimbriae of infrastaminal scales with secretory cells [internal laticifers(s)]protected by an epidermis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

2. Stigmas elongate: conical, cylindrical, terete or clavate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 32. Stigmas capitate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . IV. Subg. Grammica

3. Stigmas ± as thick as the styles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . II. Subg. Cuscuta3. Stigmas thicker than the styles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . III. Subg. Pachystigma

Cuscuta L., Sp. Pl.: 124. 1753.— TYPE: Cuscuta europaea L.(N. L. Britton et A. Brown, Ill. Fl. N. U. S. ed. 2. 3: 48. 1913;Hitchcock, Prop. Brit. Bot. 126. 1929). Cassytha S. F. Gray,Nat. Arr. Brit. Pl. 2: 345. 1821, nom. illeg, non L., 1753.

Hemi- to holoparasitic herbs, annual or perennatingthrough haustorial tissue left inside the host. Stems filiform,greenish, yellow, orange, or purple, trailing or dextrorselytwining and attached to the host by numerous smallhaustoria. Leaves rudimentary, alternate, scales. Inflores-cence units monochazial cymes further grouped in thyrsesor cymose inflorescences. Flowers bisexual, radial, (3–)4–5-merous, more or less fleshy, white, white-creamy, some-times yellow or pink to purple; laticifers commonly presentin all the flower organs, isolated or articulated, conspicuousor not; calyx and corolla gamopetalous; stamens alternat-ing with the corolla lobes, anthers longitudinally dehiscent;pollen heteromorphic, commonly 3-zonocolpate (sometimes5–12-zonocolpate), exine imperforate, perforate, microreticulateor reticulate; infrastaminal scales with secretory role usuallypresent, scale-like appendages alternating with the corollalobes, variously fimbriate, fused at the base and adnatewith the base of the corolla tube; ovary superior, 2-locular,each locule with 2 anatropous ovules; styles 1 or 2, terminal,stigmas capitate to linear. Fruits capsules, circumscissile bya ± regular line near the base, irregularly dehiscent orindehiscent. Seeds 1–4 per capsule; hilum terminal or sub-terminal; endosperm nuclear; embryo uniformly slender,without cotyledons, 1–3-coiled, rarely globose-enlarged.

I. CUSCUTA SUBG. MONOGYNELLA (Des Moul.) Peter, Engl. &Prantl, Nat. Pflanzenfam. 4(3): 38. 1891. Monogynella DesMoul., Etud. Cuscut. 65. 1853. Cuscuta [“Group”]MonogynaEngelm., Trans. Acad. Sci. St. Louis 1: 460. 1859, nom. inval.Cuscuta subg. Monogyna (Engelm.) Yunck., Mem. TorreyBot. Club 18: 248. 1932, comb. superfl.—TYPE:Monogynellavahliana (Vahl.) Des Moul. (Cuscuta monogyna Vahl).Peter made no reference to Des Moulins’s Monogynellabut indicated that the taxonomic arrangement fol-lows Engelmann. Since Engelmann stated that his“Group” Monogynella is based on Des Moulins’s (genus)Monogynella, the basionym can be attributed unequivo-cally to Des Moulins. Figures 2A–B, G.

Aplostylis Raf., Fl. Tellur. 4: 91. 1838.—TYPE: Aplostylislupuliformis (Krock.) Raf. (� Cuscuta lupuliformis Krock.).

Kadurias Raf., Fl. Tellur. 4: 91. 1838.—TYPE: Kadurias reflexa(Roxb.) Raf. (� Cuscuta reflexa Roxb.).

Cuscuta sect. Callianche Engelm., Trans. Acad. Sci. St. Louis 1:518. 1859.—TYPE: Cuscuta reflexa Roxb.

Cuscuta sect. Monostylos Maxim., Prim. Fl. Amur.: 200.1859.—TYPE: Cuscuta systyla Maxim. (= Cuscutalupuliformis Krock.).

Inflorescences ± loose thyrses: spiciform, racemiform orpaniculiform; bracts 1 at the base of cymes, 0–2 at the baseof- and sometimes on the pedicels; pedicels absent to 10 mmlong; infrastaminal scale fimbriae are glandular hairs withthe secretory cells entirely exposed; pollen 25–37.2 mm long,3–6(7)-colpate, tectum microreticulate to reticulate (excep-tion: imperforate in C. monogyna); style 1, sometimes distallybifid; stigmas variable: globose, depressed-globose, flattened,ellipsoid, ovoid, obovoid, rectangle-shaped or conical. Cap-sules circumscissile dehiscent, interstylar aperture absent.Seeds dorso-ventrally compressed, with seed coat cells ±rectangular and puzzle-like arranged, not alveolate/papillatae.Chromosome numbers: 2n = 28, 30, 32, 42, 48 (Vasudevan1975; Kaul and Bhan 1977; Pazy and Plitmann 1995; Garcıaand Castroviejo 2003).Note—Molecular data indicate that the recognition of sec-

tions in subg. Monogynella is unwarranted. AlthoughMonogynella has relatively few species (see below), the diver-sity of its flower morphology is comparable with that of themuch larger subg. Grammica (e.g. for pollen, Welsh et al.2010; gynoecium, Wright et al. 2012; and infrastaminal scales,Riviere et al. 2013). This suggests that Monogynella specieshave experienced a high degree of transgressive segregationat the same time with the adaptive radiation that followedthe evolution to parasitism in Cuscuta.Included species—This section includes 15 species: C. bucharica*

Palib. ex Fedschenko, C. cassytoides Nees, C. convallariiflora*Pavlov, C. engelmannii* Korsh, C. exaltata Engelm., C. japonicaChoisy, C. gigantea Griff., C. lehmanniana Bunge, C. lophosepala*Butkov, C. lupuliformis Krock., C. macrolepis R. C. Fang & S. H.Huang*, C. monogyna Vahl, C. pamirica* Butkov, C. reflexa


Roxb., and C. violacea Rajput & Syeda. Cuscuta chittagongensisSengupta, M. Salar Khan & Huq described from Bangladesh(Sengupta et al. 1983) is a teratological form of C. reflexa. Themost recent species described in this subgenus, Monogynellatiricensis (Chrtek 1997) from North Pakistan, appears to beclosely related to C. gigantea Griff. In general, further researchis necessary to test species limits and reveal evolutionaryrelationships within subg. Monogynella.Distribution—Most species of subg. Monogynella are

Eurasian; however, C. cassytoides is African and SoutheasternAsian, while C. exaltata is North American. Cuscuta japonica andC. reflexa have been introduced recently elsewhere through seedsused in traditional medicinal products imported from Asia.

II. CUSCUTA SUBG. CUSCUTA. Cuscuta [“Group”] CuscutaEngelm., Trans. Acad. Sci. St. Louis 1: 459. 1859, nom. inval.Cuscuta subg. Genuina Hunz., Revista Fac. Ci. Exact.13 (1): 239. 1950, nom. inval.—TYPE: Cuscuta europaea L.

Lepimenes Raf., Fl. Tellur. 4: 91. 1838.—TYPE: Lepimenesepithymum Raf. (= ?Cuscuta europaea L.)

Epilinella Pfeiff., Bot. Zeit. 3: 673. 1845.—TYPE: Epilinellacuscutoides Pfeiff. (� Cuscuta epilinumWeihe).

Epithymum Opiz, Sezman: 40. 1853.—TYPE: Epithymumcuscutoides Opiz (� Cuscuta epithymum (L.) L.).

Succuta Des Moul., Etud. Cuscut.: 74. 1853. Cuscuta subg.Succuta (Des Moul.) Yunck., Ill. Biol. Monogr. 6:111. 1921.—TYPE: Succuta alba (C. Presl.) Des Moul.(= Cuscuta epithymum (L.) L.).

Inflorescences dense, glomerulate; bracts 1 at the base ofthe inflorescences, usually absent at the base of pedicels;pedicels absent to 4.0 mm long; infrastaminal scales fimbriaewith internal laticifer(s); pollen grains 18–27 mm long, 3(12)-colpate, tectum imperforate (rarely perforate); styles 2, ±equal or stigmas sessile (lacking styles); stigmas cylindrical,terete or clavate, ± of the same thickness as the styles; cap-sules irregularly or circumscissile dehiscent or indehiscent;interstylar aperture small or inconspicuous; seeds angled tosubglobose, seed coat cells alveolate when dry and papillosewhen hydrated. Chromosome numbers: 2n = 8, 10, 14, 16, 18,20, 26, 28, 30, 32, 36, 42 (Pazy and Plitmann 1995; Garcıa andCastroviejo 2003). Figure 2C.Subgenus Cuscuta includes 21 species (see sections

below).

Key to the Sections of CUSCUTA subg. CUSCUTA

1. Styles absent or stigmas on short apical ovary projections (rostrum) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sect. Epistigma1. Styles present . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

2. Calyx not truncated, with well-developed lobes more than 0.5 mm long . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sect. Cuscuta2. Calyx truncated, without lobes or reduced to a short mucro up to 0.5 mm long . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sect. Babylonicae

1. CUSCUTA SECT. CUSCUTA. Cuscuta sect. Eucuscuta Engelm.,Trans. Acad. Sci. St. Louis 1: 460. 1859, nom. inval.Cuscuta subsect. Leptostylae Rouy, Fl. France 10: 355.1908, nom. inval. Cuscuta subsect. Europaeae Yunck.,Mem. Torrey Bot. Club 18: 274. 1932, nom. inval.—TYPE:Cuscuta europaea L.

Cuscuta subsect. Euepilinella Rouy, Fl. France 10: 354. 1908,nom. inval.—TYPE.—Epilinella cuscutoides Pfeiff. (� CuscutaepilinumWeihe.)

Cuscuta subsect. Planiflorae Yunck., Mem. Torrey Bot. Club18: 280. 1932.—TYPE: Cuscuta planiflora Ten.

Inflorescence a dense or umbellate glomerule, with a singlebasal bract, generally with more than 2 flowers. Flowers 1.4–5.0 mm long, sessile or on pedicels up to 4.0 mm long; calyxcupulate to urceolate, shorter to longer than the corolla tube,divided 1/4 to nearly to the base, lobes broadly ovate toobovate, occasionally somewhat keeled, margins entire, apexsubulate to obtuse or with a terminal or subterminal multi-cellular conical or subconical protuberance; corolla campan-ulate, tubular or urceolate, lobes shorter to longer than thetube, from broadly ovate to obovate, margins entire, apexsubulate to obtuse, sometimes cucullate or with a terminalor subterminal multicellular conical or subconical protuber-ance; infrastaminal scales present, shorter to longer thancorolla tube; pollen grains 3-colpate to 12-pantocolpate, 18–27 mm long, tectum imperforate (rarely perforate); stylescylindrical or somewhat subulate; stigmas cylindrical, tereteor clavate, ± of the same thickness as the styles. Capsulecircumcissile dehiscent (indehiscent in C. triumvirati) globoseto globose-depressed with a small to intermediate interstylaraperture. Figures 3A–C.

Note—Yuncker (1932) divided sect. Cuscuta in three sub-sections: Babylonicae, “Europeae” and Planiflorae. Whereassubsect. Babylonicae is accepted here as a different monotypicsection (see below), Europaeae and Planiflorae are notrecognised because they were based on highly homoplasiouscharacters. The phylogeny of Garcıa and Martın (2007)showed that neither of the latter subsections was monophy-letic, but three major clades were resolved for species of sect.Cuscuta. One of them included species distributed in TropicalAfrica and SW of the Arabian Peninsula. A second cladeincluded C. europaea, C. approximata, and C. balansae, and therest of the species formed the third monophyletic group. Therelationships between and within these three groups arediscussed in Garcıa and Martın (2007) and more detailedrevisions of particular groups within subg. Cuscuta can befound in Garcıa (1998, 1999, 2001).

Included Species—Section Cuscuta includes 15 species:C. abyssinica A. Rich., C. approximata Bab., C. balansae Boiss. &Reut., C. castroviejoi M. A. Garcıa, C. epilinum Weihe,C. epithymum (L.) L., C. europaea L., C. nivea M. A. Garcıa,C. palaestina Boiss., C. planiflora Ten., C. pretoriana Yunck.,C. rausii M. A. Garcıa, C. rhodesiana Yunck., C. somaliensisYunck., C. triumvirati Lange. Cuscuta mesatlantica Dobignarddescribed from Morocco (Dobignard 2009) also belongs tothis section but we could not examine the type or otherspecimens to confirm its validity. According to the descrip-tion it may be a synonym of C. epithymum or C. approximata.Other species that have been recognized in local taxonomictreatments of the genus (e.g. Butkov 1953; Feinbrun 1972;Plitmann 1978) are here considered as synonyms. Moredetailed studies, however, may suggest the recognition ofC. pellucida Butkov, C. kurdica Engelm., and C. maroccanaTrab., which we considered synonyms of C. planiflora,


C. europaea, and C. epithymum, respectively. Cuscuta obtusataEngelm. and C. letourneuxii Trab., species accepted byYuncker (1932), are known only from the type collectionsand lack clear distinctive morphological characters.

Distribution—Section Cuscuta evolved in Europe, Africa,and Asia, except the South East and Indian subcontinent.Species such as C. approximata, C. epithymum, and C. planiflorahave been introduced and naturalized in the Americas,Australia, and New Zealand.

2. CUSCUTA SECT. EPISTIGMA Engelm., Trans. Acad. Sci. St. Louis1: 471. 1859.— TYPE: Cuscuta pedicellata Ledeb., heredesignated.

Cuscuta sect. Clistococca Engelm., Trans. Acad. Sci. St. Louis 1:473. 1859.—TYPE: Cuscuta capitata Roxb.

Inflorescence in a more or less dense or umbellate glomer-ule, with a single basal bract, generally with more than2 flowers. Flowers 2.0–5.5(–6.5) mm long, sessile or on pedi-cels up to 5.0 mm long; calyx rotate or campanulate to urceo-late, shorter to longer than the corolla tube, entire or divided2/3 to the base, lobes broadly ovate to triangular or absent(calyx truncate in C. haussknechtii), somewhat keeled andfleshy to the apex, margins entire or slightly denticulate, apexsubulate to obtuse; corolla campanulate, tubular or urceolate,lobes shorter to longer than the tube, from broadly ovate toobovate, margins entire, apex subulate to obtuse; infra-staminal scales present, shorter to longer than corolla tube;pollen data not available; styles lacking; stigmas cylindricalor subulate. Capsule irregularly dehiscent (indehiscent inC. capitata) globose to globose-depressed with a small tointermediate interstylar aperture. Figure 3D.

Note—This section includes C. capitata, which Engelmann(1859) and Yuncker (1932) included in a monotypic section,Clistococca, based on its indehiscent fruits. Fruit dehiscence ishighly homoplastic in Cuscuta and indehiscent fruits are alsopresent in other species of the type subgenus, such as inC. triumvirati. At a superficial examination, the styles ofC. capitata appear developed but their conical morphology,together with the pyriform shape of the ovary indicate thatthey are apical projections of the ovary (rostrum) rather thattrue styles. Moreover, a similar morphology of the upper partof the ovary is present in other species traditionally includedin sect. Epistigma, such as C. pedicellata or C. kotschyana. Giventhe topology of the phylogenetic trees obtained by Garcıa andMartın (2007) and Garcıa et al. (2014) we consider C. capitataas a member of sect. Epistigma.

Included Species—Section Epistigma includes five species:C. capitata Roxb., C. haussknechtii Yunck., C. kotschyana Boiss.,C. pedicellata Ledeb., C. pulchella Engelm.

Distribution—Section Epistigma is distributed in Centraland Southwest Asia, as well as in Northeast Africa.

3. Cuscuta sect. Babylonicae (Yunck.) M. A. Garcıa, stat nov.Cuscuta subsect. Babylonicae Yunck., Mem. Torrey Bot.Club 18: 273. 1932.—TYPE: Cuscuta babylonica Aucherex Choisy.

Inflorescence a loose umbellate glomerule, with a singlebasal bract, generally with 1–4 (–15) flowers. Flowers 2.5–3.5 mm long, on pedicels up to 7 mm long; calyx obconic orcampanulate, shorter or as long as the corolla tube, truncatedand entire, lobes absent or reduced to acute and erect-spreading projections up to 0.5 mm long; corolla tubular

or campanulate in anthesis and urceolate in fruit, lobesabout as long as the tube, ovate to oblong, obtuse, marginsentire; infrastaminal scales present, shorter than corolla tube,with very short or almost absent fimbriae; pollen grains3(4)-colpate, 17–19 mm long, tectum imperforate; stylescylindrical or somewhat subulate; stigmas long subulate orsubcylindric, ± of the same thickness as the styles. Capsuleirregularly dehiscent, subglobose to globose-depressed witha small to intermediate interstylar aperture. Figure 3E.Note—The ITS phylogeny obtained by Garcıa and Martın

(2007) placed C. babylonica sister to the species of sect.Epistigma. This relationship was not resolved in the trnL intronphylogeny in the same study but the forced topology of thisspecies as sister to the species of sect. Cuscutawas not rejectedby a Shimodaira-Hasegawa test (Garcıa and Martın 2007).Some characters, such as the development of the first buds ofthe glomerules into floral branches instead of flowers and thefruit dehiscent by an irregular line, suggest a relationship ofthis species with sect. Epistigma. However, the developedstyles which characterize sect. Cuscuta bring C. babylonicacloser to this latter group of species. Its characteristic morphol-ogy and the unclear phylogenetic relationships are the reasonsto propose a monotypic section for this species. Cuscutababylonica has the lowest chromosome number known in thegenus (2n = 8) and the longest chromosomes known in subg.Cuscuta (up to 8 mm; Pazy and Plitmann 1987).Included Species—Sect. Babylonicae is monotypic including

only C. babylonica Aucher ex Choisy.Distribution—Cuscuta babylonica is distributed in Central

and West Asia but more common in Iraq.

III. CUSCUTA SUBGEN. PACHYSTIGMA (Engelm.) Baker & C. H.Wright, Thiselton-Dyer (ed.), Fl. Cap. 4(2): 84. 1904.Cuscuta sect. Pachystigma Engelm., Trans. Acad. Sci.St. Louis 1: 474. 1859. Cuscuta subsect. Africanae Yunck.,Mem. Torrey Bot. Club 18: 263. 1932.—TYPE: Cuscutaafricana Willd. Cuscuta subsect. Cucullatae Yunck., Mem.Torrey Bot. Club 18: 263. 1932.—TYPE: Cuscuta cucullataYunck. (= Cuscuta gerrardii Baker).

Inflorescence ± loose paniculiform, bracts 1 at the base ofclusters, 1 at the base of pedicels; pedicels to 8 mm long;infrastaminal scales fimbriae with internal laticifer(s); pollengrains 3(4)-colpate, 22–30 mm long, tectum imperforate toperforate; styles 2, equal or slightly unequal, cylindrical,oblong or conical, thicker than the styles. Capsules circum-scissile, interstylar aperture inconspicuous; seed coat cellscommonly alveolate when dried and papillose whenhydrated. Figures 2D, 3F.Note—Although Pachystigma was proposed as a subgenus

by Baker and Wright (1904) more than a century ago, this isthe first time it is accepted (see Introduction). No morpholog-ical characters have been found to further divide this smallsubgenus into different sections. The tree topologies obtainedby Garcıa et al. (2014) also indicate that the recognition ofsections in subg. Pachystigma is unnecessary. Yuncker (1932)recognized the monotypic subsect. Cucullatae based on theindehiscent fruits of C. cucullata. Yuncker mentioned thatC. gerrardii may also belong to that subsection. After study-ing the types and a few more recent collections we considerthat C. cucullata and C. gerrardii are conspecific.Included Species—Subgenus Pachystigma includes five spe-

cies: C. africanaWilld., C. angulata Engelm., C. gerrardii Baker,C. natalensis Baker, C. nitida E. Mey. ex Choisy.


Distribution—Subgenus Pachystigma is confined to SouthAfrica and it is more common in the coastal regions ofWestern Cape, Eastern Cape, and Natal provinces. Cuscutagerrardii also occurs in Swaziland.

IV. CUSCUTA SUBG. GRAMMICA (Lour.) Peter, Engl. & Prantl, Nat.Pflanzenfam. 4(3): 38. 1891. Grammica Lour. Fl. Cochinch.170. 1790 [“Grmmica”].—TYPE: Grammica aphylla Lour.(= Cuscuta chinensis Lam.).

Anthanema Raf., Fl. Tellur. 4: 90. 1838.—TYPE: Anthanemaparadoxa (Raf.) Raf. (� Cuscuta paradoxa Raf.; designatedby Manitz 1976)

Dactylepis Raf. Fl. Tellur. 4: 125. 1838.—TYPE: Dactylepisbrownei Raf. (= ?Cuscuta americana L.; Yuncker 1932)

Eronema Raf. Fl. Tellur. 4: 125. 1838.— TYPE: Eronemarobinsoni Raf. (= ?Cuscuta americana L.; Yuncker 1932)

Kadula Raf., Fl. Tellur. 4: 90. 1838.—TYPE: Kadulacorymbosa (Ruiz & Pav.) Raf. (� Cuscuta corymbosaRuiz & Pav.).

Nemepis Raf., Fl. Tellur. 4: 91. 1838.— TYPE: Nemepis odorata(Ruiz & Pav.) Raf. (� Cuscuta odorata Ruiz & Pav., desig-nated by Manitz 1976)

Pentake Raf., Fl. Tellur. 4: 90. 1838.—TYPE: Pentake chinensis(Lam.) Raf. (� Cuscuta chinensis Lam.).

Lepidanche Engelm., Amer. J. Sci. Arts 43: 343. 1842.—TYPE:Lepidanche compositarum Engelm. (= Cuscuta glomerataChoisy).

Engelmannia Pfeiff., Bot. Zeitung (Berlin) 3: 673. 1845.—TYPE: Engelmannia migrans Pfeiff. (= Cuscuta suaveolensSer.).

Cuscutina Pfeiff., Bot. Zeitung (Berlin) 4: 492. 1846.—TYPE:Cuscutina suaveolens Pfeiff. (= Cuscuta suaveolens Ser.).Also proposed as a substitute name for Engelmannia.

Pfeifferia Buching. in Ann. Sci. Nat., Bot., ser. 3, 5: 88.1846.—TYPE: Pfeifferia suaveolens Buching. (= Cuscutasuaveolens Ser.).

Buchingera F. W. Schultz, Jahrb. Pract. Pharm. VerwandteFacher 14: 170. 1847.—TYPE: Buchingera suaveolens F.W.Schultz. (= Cuscuta suaveolens Ser.). Buchingera was pro-posed as a substitute name both for Engelmannia Pfeiff.1845, non A. Gray ex Nuttall 1840 (Asteraceae) and forPfeifferia J. D. Buchinger 1846, non Pfeifferia Salm-Dyck1845 (Cactaceae).

Cuscuta [“Group”] Grammica Engelm., Trans. Acad. Sci.St Louis 1(3): 459. 1859, nom. inval.

Inflorescences dense to loose, glomerulate, paniculiform,umbelliform, corymbiform, fasciculate or racemiform; bracts1–3 at the base of the clusters, 0–10 at the base of- and on thepedicels; pedicels absent to 12 mm; infrastaminal scales fim-briae with internal laticifer(s), very variable, sometimesentirely reduced; pollen grains 13–30 mm long, 3(4)-colpate,tectum imperforate, perforate, microreticulate (7–8-colpateand reticulate in some species of sect. Subulatae); styles 2, ±unequal; stigmas capitate (globose, depressed, flattened orellipsoid); capsules circumscissile dehiscent or indehiscent;interstylar aperture inconspicuous to large; seeds globose toovoid, angled or dorsoventrally compressed; seed coat cellscommonly alveolate when dried and papillose when hydrated.Chromosome numbers: 2n = 28, 30, 32, 38, 44, 56, 60 (Fogelberg1938; Pazy and Plitmann 1995; Garcıa and Castroviejo 2003).Figures 2E–F, H.Subgenus Grammica includes 153 species (see sections

below).

Key to the Sections of Subgenus GRAMMICA

1. Embryo spherically enlarged . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sect. Denticulatae1. Embryo filiform, not spherically enlarged . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

2. Styles thick, 0.3–0.9 mm in diameter, cylindrical or subulate; pollen grains with microreticulate orreticulate exine (exceptions with imperforate or tectum perforate are possible); stigmas large(0.25–0.6 mm in diameter) and/or lobed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3

3. Calyx and/or corolla lobes with conical or cylindrical subterminal, dorsal multicellular appendages . . . . . . . . . . . . . . . . . . . Sect. Ceratophorae3. Corolla lobes without conical or cylindrical appendages; when appendages are present on the calyx,

they are crest-like along the midvein/carena of lobes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 44. Fimbriae of infrastaminal scales often papillatae; S America (2 sp. in Africa) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sect. Subulatae4. Fimbriae of infrastaminal scales not papillatae; N America (2 sp. in Australia) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sect. Lobostigmae

2. Styles thin, 0.1–0.2 mm in diameter, cylindrical; pollen grains with perforate or imperforate tectum;stigmas small (0.1–0.25 mm in diameter), not lobed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

5. Flowers elongated; calyx and corolla divided ca. 1/4 the length . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 66. Calyx cylindrical viewed in cross-section; infrastaminal scales 3/4 to equalling corolla tube . . . . . . . . . . . . . . . . . . . . . . . .Sect. Obtusilobae6. Calyx pentagonal viewed in cross-section; infrastaminal scales 1/2 of the corolla tube . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Sect. Prismaticae

5. Flowers more or less spherical or wider than long; calyx and corolla divided 1/2 to the base(if flowers are elongated, calyx and corolla are deeply divided) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7

7. Capsules dehiscent [indehiscent in C. vandevenderi, C. columbiana (sect. Gracillimae), C. acuta,and C. membranacea (sect. Umbellatae); C. yucatana (sect. Grammica)] . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .8

8. Inflorescence glomerulate (umbellate in C. yucatana but fruit indehiscent) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sect. Grammica8. Inflorescences umbellate or corymbiform (glomerulate in C. punana, sect. Gracillimae;

C. odontolepis, sect. Umbellatae). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 99. Stems disappear at flowering time and inflorescences seem to emerge from the host’s stems . . . . . . . . . . . . . . . . . Sect. Gracillimae9. Some stems persist at flowering time and bear inflorescences . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .Sect. Umbellatae

7. Capsule indehiscent (dehiscent in C. partita of sect. Partitae) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .1010. Calyx lobes acute . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

11. Flowers with numerous bracts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sect. Oxycarpae (in part)11. Flowers with 0–1 bracts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12

12. Corolla lobes inflexed . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sect. Indecorae12. Corolla lobes straight . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13

13. Calyx divided nearly to the base; S America . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sect. Partitae13. Calix divided 1/2–2/3; Western N America . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sect. Californicae


10. Calyx lobes obtuse or rounded . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1414. Inflorescence glomerulate; corolla lobes inflexed; capsule depressed-globose,

not narrowed distally, with conspicuous interstylar aperture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sect. Cleistogrammica14. Inflorescence paniculiform; corolla lobes straight; capsule globose narrowed

or thickened apically; interstylar aperture inconspicuous . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1515. North America . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sect. Oxycarpae (in part)15. South America . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Sect. Racemosae

4. CUSCUTA SECT. GRAMMICA. Cuscuta sect. “Eugrammica”Engelm., Trans. Acad. Sci. St. Louis 1: 476. 1859, in part,nom. inval.—TYPE: Grammica aphylla Lour. (= Cuscutachinensis Lam.).

Cuscuta subsect. Obtusilobae Engelm., Trans. Acad. Sci.St. Louis 1: 476. 1859, in part.—TYPE: Cuscuta americanaL., here designated.

Cuscuta subsect. Tinctoriae Yunck., Mem. Torrey Bot. Club 18:208. 1932, in part (only C. chinensis Lam.).—TYPE:Cuscuta tinctoraMart.

Cuscuta subsect. Odontolepisae Yunck., Mem. Torrey Bot. Club18: 226. 1932, in part (C. dentatasquamata Yunck, C.potosina W. Schaffn. ex Engelm.).—TYPE: Cuscutaodontolepis Engelm.

Cuscuta subsect. Acutae Yunck., Mem. Torrey Bot. Club 18:152. 1932, in part (C. palustris Yunck. and C. yucatanaYunck).—TYPE: Cuscuta acuta Engelm.

Inflorescence glomerulate (umbellate in C. yucatana).Flowers 1.5–4 mm long; calyx cupulate, ca. as long as thecorolla tube, divided 1/2–2/3 to the base, lobes broadly tri-angular-ovate, carinate or with stomatiferous multicellularprotuberances along mid-veins, margins entire, apex acuteto ± obtuse; corolla campanulate; lobes equaling the tube,apex acute to ± obtuse, not inflexed; infrastaminal scalespresent, equaling or longer than corolla tube; pollen grains3(4)-colpate, tectum imperforate; styles cylindrical, thin (0.1–0.2 mm in diameter); stigmas globose (0.1–0.25 mm in diame-ter). Fruit dehiscent (indehiscent in C. yucatana) globose toglobose-depressed (ovoid in C. potosina), with small interstylaraperture. Figures 3G–H.

Note—The composition of this group is essentially newbecause its species were included by Yuncker (1932, 1965) inthree different subsections (Fig. 1): C. applanata and C. chinensisin subsect. Tinctoriae; C. potosina in subsect. Odontolepisae (bothsubsections classified in sect. Eugrammica; Yuncker 1932), andC. yucatana in subsect. Acutae (sect. Cleistogrammica; Yuncker1932). Costea et al. (2011b) added to this clade a new species,C. azteca, and reinstated C. alata, previously considered syn-onymous to C. applanata (Yuncker 1932, 1965). Moreover,Costea et al. (2011b) found C. chinensis and C. applanata torepresent one single species.

Included Species—Section Grammica includes seven species:C. alata Brandegee, C. azteca Costea & Stefanovic, C. chinensisLam., C. dentatasquamata Yunck.*, C. palustris Yunck.*, C. potosinaW. Schaffn. ex Engelm., and C. yucatana Yunck.

Distribution—Section Grammica is distributed in SouthernU. S. A. and Mexico, with C. chinensis var. chinensis having adisjunct distribution in Australia and Asia, most likely as aresult of relatively recent long-distance dispersal (Costeaet al. 2011b).

5. Cuscuta sect. Subulatae (Engelm.) Costea & Stefanovic,stat. nov. Cuscuta subsect. Subulatae Engelm., Trans.Acad. Sci. St. Louis 1: 476. 1859, in part (all the species

except C. jalapensis).—TYPE: Cuscuta grandiflora Kunth,here designated. Cuscuta subsect. Grandiflorae Yunck.,Mem. Torrey Bot. Club 18: 183. 1932.—TYPE: Cuscutagrandiflora Kunth

Cuscuta subsect. Odoratae Yunck., Mem. Torrey Bot. Club 18:188. 1932.—TYPE: Cuscuta odorata Ruiz & Pav.

Cuscuta subsect. Odontolepisae Yunck., Mem. Torrey Bot. Club18: 226. 1932, in part (C. cockerellii and C. hitchcockii).—TYPE: Cuscuta odontolepis Engelm.

Cuscuta subsect. Acutilobae Yunck., Mem. Torrey Bot. Club18: 201. 1932, in part (all spp. except C. xanthochortosMart.).—TYPE: Cuscuta acutiloba Engelm.

Cuscuta subsect. Oxycarpae Engelm., Acad. Sci. St. Louis 1:499. 1859, in part (only C. cristata Engelm.).—TYPE:Cuscuta gronoviiWilld., here designated.

Cuscuta subsect. Platycarpae Engelm. ex Yunck., Mem. TorreyBot. Club 18: 124. 1932, in part (only C. cristata Engelm.).—TYPE: Cuscuta obtusiflora Kunth, here designated.

Cuscuta subsect. Lepidanchiopsis Yunck., Ill. Biol. Monogr. 6:119. 1921, in part (all spp. except C. strobilacea Liebm.).—TYPE: Cuscuta bracteata Engelm., here designated.

Cuscuta subsect. Denticulatae Yunck., Mem. Torrey Bot. Club18: 170. 1932, in part (only C. microstyla Engelm.).—TYPE: Cuscuta denticulata Engelm.

Inflorescences glomerulate (fasciculate or umbellate inC. grandiflora, C. argentinana, C. friesii). Flowers are amongthe largest in subg. Grammica, 4–9 mm, often fleshy, thickand sometimes fragrant (exceptions: C. argentinana andC. microstyla have relatively small flowers, 2–3 mm long);calyx cupulate to campanulate, 1/4 to equalling corolla tube,divided 1/2–2/3, with lobes acute to rounded, overlappingor not; corolla cupulate, globose or cylindrical with lobesacute to rounded; infrastaminal scales diverse (absent inC. grandiflora), commonly with papillae on the fimbriae;pollen grains 3(4) or 6–7-colpate, tectum imperforate, per-forate, microreticulate, or reticulate; styles cylindrical, thick(0.2–0.9 mm in diameter), stigmas large (0.25–0.6 mm indiameter), usually lobed; fruit dehiscent (indehiscent inC. cristata). Figures 3I–L.Note—Subulatae is the largest section of subg. Grammica

and of Cuscuta in general. The group included inEngelmann’s view all the species with thick and/or subulatestyles regardless of the shape of their calyx/corolla lobes.With the exception of C. jalapensis which does not belong tothis clade (see section Lobostigmae), this is also largely thespecies composition of clade O that resulted from our phylo-genetic studies (Stefanovic et al. 2007; Garcıa et al. 2014).Yuncker (1932), however, left C. jalapensis in subsectionSubulatae together with several newly described related spe-cies with subulate styles fromMexico, which belong to sectionLobostigmae, and redistributed the species of Engelmann’ssubsect. Subulatae among three new subsections (Grandiflorae,


Odoratae, and Acutilobae; Fig. 1). Several species with numer-ous bracts at the base of the flower, a morphological trait thatalso evolved in the sections Ceratophorae andObtusiflorae, weregrouped by Yuncker (1921) in a new section, Lepidanchopsis.Cuscuta cristata, which is also a part of sect. Subulatae, wasincluded by both Engelmann (1859) and Yuncker (1932) insect. Cleistogrammica because of its indehiscent capsules.Included Species—Section Subulatae includes 29 species

and possibly two additional ones that need confirmation(see below): C. acutiloba Engelm.*, C. alatoloba Yunck.*,C. argentinana Yunck., C. bella Yunck., C. boliviana Yunck.,C. bracteata Engelm.*, C. chilensis Ker Gawl., C. cockerelliiYunck., C. cristata Engelm., C. foetida Kunth, C. friesii Yunck.,C. flossdorfii Hicken, C. goyaziana Yunck.*, C. hitchcockii*,C. kilimanjari Oliv., C. grandiflora Kunth, C. globiflora Engelm.,C. lucidicarpa Yunck., C. microstyla Engelm., C. odorata Ruiz &Pav., C. orbiculata Yunck., C. paitana Yunck., C. parodianaYunck., C. pycnantha Benth., C. purpurata Phil., C. rotundifloraHunz., C. rubella Yunck., C. serrata Yunck.*, C. tucumanaYunck.*. Based on their morphology, C. blepharolepis Welw.ex Hiern*, C. rustica Hunz., known only from their types,may also be a part of this clade but we were not as confidentabout their placement as in the case of the rest of the species.Distribution—Section Subulatae is South American except

for C. kilimanjari and possibly C. blepharolepis, which areAfrican. Biogeographical scenarios of long-distance dispersalin subg. Grammica were discussed by Garcıa et al. (2014).

6. Cuscuta sect. Obtusilobae (Engelm.) Costea & Stefanovic,stat nov. Cuscuta subsect. Obtusilobae Engelm., Trans.Acad. Sci. St. Louis 1: 479. 1859, in part.—TYPE: Cuscutaamericana L., here designated. Cuscuta subsect. AmericanaeYunck., Mem. Torrey Bot. Club 18: 217. 1932.—TYPE:Cuscuta americana L.

Inflorescences glomerulate or dense paniculiform. Flowers3–7 mm long; calyx cylindrical (round in cross-section), 3/4to equalling corolla tube, divided ca. 1/4 the length, withrounded lobes; corolla cylindrical, lobes ca. 1/4 of the corollatube, rounded; infrastaminal scales 3/4 to equaling corollatube; pollen grains 3(4)-colpate, tectum imperforate (perfo-rate in C. macrocephala); styles cylindrical, thin; stigmas small.Fruit dehiscent, globose to ovoid. Figures 3M–N.Note—Engelmann (1859) circumscribed Subsect. Obtusilobae

to includemanymore species; our delimitation approaches hisinformal (unranked) subgroup of taxa with “elongatedflowers”. Yuncker (1932) maintained this core of species as asubsection, Americanae (Fig. 1).Included Species—Section Obtusilobae includes four spe-

cies: C. americana L., C. cozumeliensis Yunck., C. globulosaBenth., and C. macrocephalaW. Schaffn. ex Yunck.Distribution—The section is distributed in the U. S. A.

(Florida), Mexico, West Indies, Central and South America.

7. Cuscuta sect. Prismaticae (Yunck.) Costea & Stefanovic,stat nov. Cuscuta subsect. Prismaticae Yunck., Mem.Torrey Bot. Club 18: 225. 1932.—TYPE: Cuscuta prismaticaPav. ex Choisy.

Inflorescences glomerulate or dense paniculiform. Flowers4–7 mm long; calyx campanulate-cylindrical, angled (pen-tagonal in cross-section), 1/2–3/4 of the corolla tube,divided ca. 1/4 of its length, with rounded or acute lobes;corolla cylindrical, lobes ca. 1/4 of the corolla tube, roundedor acute; infrastaminal scales ca. 1/2 of the corolla tube;

pollen grains 3(4)-colpate, tectum imperforate; styles cylindri-cal, thin; stigmas small. Fruit dehiscent, globose. Figure 3O.

Note—Subsection Prismaticae included originally onlyC. prismatica (Yuncker, 1932). We have found that this spe-cies is closely related to C. corymbosa, not to C. americana(Stefanovic et al. 2007; Garcıa et al. 2014) and its relativesas suggested by both Engelmann (1859) and Yuncker (1932).This section resembles morphologically sect. Obtusilobaebut differs in the pentagonal calyx (lobes are flat formingthe faces of a pentagonal prism) and infrastaminal scalesca. 1/2 the length of the corolla tube.

Included Species—Section Prismaticae includes only twospecies: C. corymbosa Ruiz & Pav. and C. prismatica Pav.ex Choisy.

Distribution—Members of this section are distributed inMexico, Central, and South America.

8. Cuscuta sect. Ceratophorae (Yunck.) Costea & Stefanovic,stat. nov. Cuscuta subsect. Ceratophorae Yunck., Ill. Biol.Monogr. 6: 116. 1921.—TYPE: Cuscuta boldinghii Urban(= C. ceratophora Yunck.).

Cuscuta subsect. Lepidanchopsis Yunck., Ill. Biol. Monogr. 6:119. 1921, in part (only C. strobilacea Liebm.).—TYPE:Cuscuta strobilacea Liebm., here designated.

Cuscuta subsect. Odontolepisae Yunck., Mem. Torrey Bot. Club18: 226. 1932, in part. (C. costaricensis Yunck., C. orteganaYunck.).—TYPE: C. odontolepis Engelm.

Cuscuta subsect. Tinctoriae Yunck., Mem. Torrey Bot. Club 18:208. 1932, in part (C. mexicana Yunck.).—TYPE: CuscutatinctoriaMart.

Inflorescences glomerulate to corymbiform. Flowers 3–7 mm long; calyx cupulate, campanulate or tubular ca. 1/2to longer than corolla tube, divided nearly to the base, withentire or variously denticulate lobes; corolla tube campanu-late to cylindrical (ovoid to urceolate in C. carnosa), lobesacute to rounded. Both calyx and corolla lobes commonly withdorsal, subterminal conical or cylindrical multicellularappendages with stomata (absent on the corolla of C. carnosa);infrastaminal scales diverse; pollen grains 3(4)-colpate, tectumimperforate, perforate or microreticulate; gynoecia with thick,subulate or cylindrical styles and large, globose stigmas. Fruitdehiscent. Figures 3P–S.

Note—In the past, subsect. Ceratophorae comprised only fourspecies: C. chapalana, C. erosa, C. boldinghii, and C. blepharolepis(Yuncker 1921; 1932). Cuscuta blepharolepis, known only fromits type, could not be sampled for the molecular studies butbased on its morphology is more likely to be a member ofsection Subulatae. Our results have shown that four other spe-cies, C. strobilacea, C. mexicana, C. costaricensis, and C. ortegana,previously included by Yuncker (1932, 1965) in the subsec-tions Lepidanchopsis, Tinctoriae, and Odontolepisae, are alsomembers of sect. Ceratophorae (Fig. 1; Stefanovic et al. 2007),together with two new species, C. bonafortunae and C. carnosa(Costea et al. 2011a).

Included Species—Section Ceratophorae comprises ninespecies: C. boldinghii Urb., C. bonafortunae Costea & I. Garcıa,C. carnosa Costea and Stefanovic, C. chapalana Yunck.,C. costaricensis Yunck., C. erosa Yunck., C. mexicana Yunck.,C. ortegana Yunck., and C. strobilacea Liebm.

Distribution—The section is distributed in SouthernU. S. A., Mexico, West Indies, Central America, and North-ern South America.


9. Cuscuta sect. Umbellatae (Yunck.) Costea & Stefanovic,stat. nov. Cuscuta subsect. Umbellatae Yunck., Mem.Torrey Bot. Club 18: 234. 1932, in part (see Note)—TYPE:Cuscuta umbellata Kunth.

Cuscuta subsect. Leptanthae Yunck., Mem. Torrey Bot. Club18: 242. 1932.—TYPE: Cuscuta leptantha Yunck.

Cuscuta subsect. Odontolepisae Yunck., Mem. Torrey Bot. Club18: 226. 1932, in part (C. odontolepis Engelm.).—TYPE:Cuscuta odontolepis Engelm.

Cuscuta subsect. Acutae Yunck., Mem. Torrey Bot. Club 18:152. 1932, in part (C. acuta Engelm. and C. membranaceaYunck.).—TYPE: Cuscuta acuta Engelm.

Inflorescences umbelliform or fasciculate. Flowers 2–5 mmlong (to 7.5 mm in C. polyanthemos); calyx campanulate tocylindrical, 1/4 to equaling the length of the corolla tube,divided 1/3–1/2 the length, with acute lobes; corolla tubecampanulate to cylindrical with acute lobes; infrasta-minal scales commonly equalling corolla tube (absent inC. hyalina); pollen grains 3(4)-colpate, tectum imperforateor perforate; styles cylindrical, thin; stigmas globose, small.Fruit dehiscent (indehiscent in C. acuta and C. membranacea).Figures 3T–U.

Note—The evolutionary history of this section involvedhybridization and long-distance dispersal (Stefanovic andCostea 2008; Costea and Stefanovic 2010). Section Umbellataeincludes in our view a part of the former subsect. Umbellataein which Yuncker (1932, 1965) grouped nine species charac-terized by umbellate inflorescences and dehiscent capsules(C. umbellata, C. deltoidea, C. desmouliniana, C. fasciculata, C.gracillima, C. hyalina, C. lacerata, C. macvaughii, C. saccharata,and C. serruloba). Phylogenetic studies indicated a need forradical reorganization of this group. First, C. gracillima,C. sidarum (= C. saccharata), and C. deltoidea (= C. serruloba)form a separate infrageneric group (see sect. Gracillimae;Stefanovic et al. 2007; Costea et al. 2008a). Second, five otherspecies previously included in various sections and subsec-tions of subg. Grammica are also a part of this clade/section(Stefanovic et al. 2007; Costea and Stefanovic 2010; Fig. 1).Two of these, C. acuta and C. membranacea, have indehiscentcapsules (previously included in sect. Eugrammica, subsect.Acutae; Yuncker 1932; Hunziker 1949), while the rest havecircumscissile capsules: C. odontolepis (formerly in sect.Eugrammica, subsect. Odontolepisae; Yuncker 1932), C. tuberculata,C. leptantha, and C. polyanthemos (formerly in sect. Eugrammica,subsect. Leptanthae; Yuncker 1932). Finally, two new species,C. liliputana and C. legitima, were recently described fromsouthern U. S. A. and Mexico (Stefanovic and Costea 2008;Costea and Stefanovic 2010). Cuscuta appendiculata fromSouth Africa was included by Yuncker (1932) in subsectionAcutae. To date, in subg. Grammica, only the sectionsSubulatae and Umbellatae are known to have representativesin Africa. Morphologically, C. appendiculata may belong tosect. Umbellatae but we could not sample it for the molecularstudies. A closer examination of the specimens used byStefanovic et al. (2007) for C. appendiculata revealed that theybelong to C. gerrardii (Garcıa et al. 2014).

Included Species—Section Umbellatae comprises 13 species:C. acuta Engelm., ?C. appendiculata Engelm.*, C. desmoulinianaYunck., C. hyalina Roth, C. lacerata Yunck.*, C. legitima Costea& Stefanovic, C. leptantha Engelm., C. liliputana Costea &Stefanovic, C. membranacea Yunck., C. odontolepis Engelm.,

C. polyanthemosW. Schaff. ex Yunck., C. tuberculata Brandegee,and C. umbellata Kunth.Distribution—SectionUmbellatae is distributed in Southern

U. S. A., Mexico, and West Indies (8 sp.); South America(3 sp.); Asia, East and Southeast Africa (C. hyalina and possi-bly C. appendiculata).

10. Cuscuta sect. Gracillimae Costea & Stefanovic, sect.nov.—TYPE: Cuscuta gracillima Engelm.

Cuscuta subsect. Umbellatae Yunck., Mem. Torrey Bot.Club 18: 234. 1932, in part (see Note).—TYPE: Cuscutaumbellata Kunth

Cuscuta subsect. Odontolepisae Yunck., Mem. Torrey Bot. Club18: 226. 1932, in part (only C. choisiana Yunck.).—TYPE:Cuscuta odontolepis Engelm.

Cuscuta subsect. Californicae Yunck., Mem. Torrey Bot. Club18: 156. 1932 (in part, only C. insquamata Yunck.).—TYPE: Cuscuta californica Choisy.

Resembling morphologically sect. Umbellatae but differingin its stems that disappear at flowering stage when the para-site is often represented only by the spherical umbelliforminflorescences that emerge directly from the host’s stem.Inflorescences umbelliform or corymbiform. Flowers 1.6–

5.5 mm long; calyx campanulate to cylindrical, equaling orexceeding the corolla tube, divided 1/3–1/2 the length, lobesacute; corolla tube campanulate to cylindrical with acutelobes; infrastaminal scales equalling or exceeding corollatube; pollen grains 3(4)-colpate, tectum imperforate or perfo-rate; styles cylindrical, thin; stigmas globose, small. Fruitdehiscent (indehiscent in C. vandevenderi). Figures 4A–C.Note—Section Gracillimae is a segregate of the former

subsect. Umbellatae (see above; Yuncker 1932; Costea et al.2008a). The position of C. macvaughii remained unresolvedin our phylogeny (Garcıa et al. 2014): while the parsimonyanalysis placed this species as sister to sect. Gracillimae, asister relationship with sect. Indecorae was recovered inBayesian and maximum likelihood trees, however, in allcases with low support (Garcıa et al. 2014). Morphologically,this species shares strong affinities with both sections but themorphology of inflorescences brings C. macvaughii closer tosection Gracillimae.Included Species—Section Gracillimae includes nine spe-

cies: C. choisiana Yunck.*, C. gracillima Engelm., C. colombianaYunck., C. deltoidea Yunck., C. insquamata Yunck.*, C.macvaughii Yunck., C. punana Costea & Stefanovic, C. sidarumLiebm., C. vandevenderi Costea & Stefanovic.Distribution—Members of sect. Gracillimae are distributed

in Mexico, Central, and South America.

11. CUSCUTA SECT. CLEISTOGRAMMICA Engelm. [“Clistogrammica”],Trans. Acad. Sci. St Louis 1: 490. 1859. Cuscuta subsect.Platycarpae Engelm. ex Yunck., Mem. Torrey Bot. Club 18:124. 1932, in part (all spp. except C. cristata Engelm. andC. victoriana Yunck.).—TYPE: Cuscuta obtusiflora Kunth,here designated. Cuscuta subsect. Obtusiflorae Hunz.,Revista Fac. Ci. Exact. 12 (4): 1124–1125. 1949.—TYPE:Cuscuta obtusiflora Kunth

Cuscuta subsect. Arvenses Yunck., Mem. Torrey Bot. Club 18: 134.1932.—TYPE: Cuscuta pentagona Engelm., here designated.

Cuscuta subsect. Indecorae Yunck., Mem. Torrey Bot. Club 18:161. 1932, in part (only C. stenolepis Engelm.).—TYPE:Cuscuta indecora Choisy


Cuscuta subsect. Californicae Yunck., Mem. Torrey Bot. Club18: 156. 1932 (in part, only C. sandwichiana Choisy).—TYPE: Cuscuta californica Choisy.

Inflorescences glomerulate to dense paniculiform orcorymbiform. Flowers 2–4 mm long; calyx cupulate to cam-panulate, equalling corolla tube, divided 1/2–2/3 the length;lobes obtuse or rounded; corolla campanulate, corolla lobesobtuse to acute, inflexed or cucullate; infrastaminal scalesequalling or exceeding corolla tube (undergoing a reductiontrend in C. australis); pollen grains 3(6)-colpate, tectumimperforate or perforate; styles cylindrical, thin; stigmas glo-bose, small. Fruit indehiscent, depressed-globose or globosewith the withered corolla remaining around it, or at the base.Figures 4D–G.Note—Engelmann’s (1859) delimitation of sect. Cleistogrammica

included all the Grammica species with indehiscent capsuleswith the exception of C. tasmanica. In its current composition,this section groups together most of the species placed byYuncker (1932) in two subsections: Platycarpae and Arvenses(Fig. 1). The evolution of this group involved hybridizationand long-distance dispersal (Stefanovic et al. 2007; Stefanovicand Costea 2008; Garcıa et al. 2014).Included Species—Section Cleistogrammica comprises 15

species: C. australis R. Br., C. bifurcata Yunck., C. campestrisYunck., C. harperi Small, C. glabrior (Engelm.) Yunck.,C. gymnocarpa Engelm., C. karatavica Pavl.*, C. pentagonaEngelm., C. plattensis A. Nelson, C. polygonorum Engelm.,C. runyonii Yunck., C. obtusiflora Kunth, C. sandwichianaChoisy, C. schlechteri Yunck., and C. stenolepis Engelm. (thelatter thought by Yuncker 1932 to belong to section Indecorae).Distribution—Cleistogrammica is the section of subg.

Grammica with the most complex biogeography. While mostof its species are North American (Costea et al. 2006a;Stefanovic et al. 2007, Garcıa et al. 2014), long-distance dis-persal was documented on all the other continents: SouthAmerica (C. gymnocarpa, C. stenolepis, and in part C. obtusiflora),Africa (C. bifurcata and C. schlechteri), Asia, Australia andEurope (C. australis, C. karatavica). In addition, C. campestrishas been recently dispersed worldwide as a seed contaminantof forage legume crops (Costea and Tardif 2006).

12. Cuscuta sect. Californicae (Yunck.) Costea & Stefanovic,stat. nov. Cuscuta subsect. Californicae Yunck., Mem.Torrey Bot. Club 18: 156. 1932.—TYPE: Cuscuta californicaChoisy.

Cuscuta subsect. Subinclusae Yunck., Mem. Torrey Bot. Club18: 165. 1932, in part (all species except C. micranthaChoisy).—TYPE: Cuscuta subinclusa Dur. & Hilg.

Cuscuta subsect. Racemosae Yunck., Mem. Torrey Bot. Club 18:143. 1932, in part (only C. decipiens Yunck.).—TYPE:Cuscuta racemosaMart.

Inflorescences glomerulate to umbelliform. Flowers 2–7 mm long; calyx campanulate to cylindrical 1/2 to equallingor exceeding corolla tube, divided 1/3–1/2 the length, lobesacute (rounded in C. decipiens); corolla campanulate, cylin-drical or globose, lobes acute (rounded in C. decipiens); infra-staminal scales show a reduction trend from well-developedin C. decipiens and C. draconella to absent in C. californica,C. brachycalyx, C. jepsonii, and C. occidentalis; pollen grains3(4)-colpate, tectum imperforate or perforate; styles cylin-drical, thin; stigmas globose, small. Fruit indehiscent,globose to ovoid. Figures 4H–I.

Note—The current delimitation of section Californicaeamalgamates Yuncker’s (1932) subsections Californicae andSubinclusae (Fig. 1). Cuscuta micrantha, placed by Yuncker(1932) in subsect. Subinclusae, belongs to sect. Racemosae(Stefanovic et al. 2007; Garcıa et al. 2014). Two new species,C. draconella and C. pacifica, and a species formerly includedby Yuncker (1932) in subsection Racemosae, C. decipiens, werealso placed by molecular studies in this section (Costea andStefanovic 2009b).

Included Species—Section Californicae has 11 species:Cuscuta brachycalyx Yunck., C. californica Hook. & Arn.,C. decipiens Yunck., C. draconella Costea & Stefanovic,C. howelliana P. Rubtzoff, C. jepsonii Yunck., C. occidentalisMillsp., C. pacifica Costea & M. A. R. Wright, C. salina Engelm.,C. subinclusa Durand & Hilg., C. suksdorfii Yunck.

Distribution—Members of this section are confined toSouthwestern North America.

13. Cuscuta sect. Indecorae (Yunck.) Costea & Stefanovic,stat. nov. Cuscuta subsect. Indecorae Yunck., Mem. TorreyBot. Club 18: 161. 1932, in part (all species exceptC. stenolepis Engelm.).—TYPE: Cuscuta indecora Choisy

Inflorescences paniculate or corymbiform. Flowers 2–5 mm long, fleshy because of dome-like epidermal cells (papil-lae also commonly present); calyx campanulate, equalling orexceeding corolla tube, divided 1/2–2/3 of the length, lobesacute; corolla campanulate, urceolate or globose, corollalobes acute with inflexed tips; infrastaminal scales equallingcorolla tube or showing a reduction trend (e.g. C. warneri);pollen grains 3(4)-colpate, tectum imperforate; styles cylin-drical, thin; stigmas globose, small. Fruit indehiscent, globoseto depressed, with a thickened apex or interstylar aperture.Figures 4J–K.

Included Species—Section Indecorae includes three species:C. indecora Choisy, C. coryli Engelm., C. warneri Yunck.

Distribution—The species of this section are NorthAmerican. Cuscuta indecora has been further dispersed as aweed of forage legumes in South America.

14. Cuscuta sect. Oxycarpae (Engelm. ex Yunck.) Costea &Stefanovic, stat. nov. Cuscuta subsect. Oxycarpae Engelm.ex Yunck., Mem. Torrey Bot. Club 18: 172. 1932.—TYPE:Cuscuta gronoviiWilld., here designated.

Cuscuta subsect. Cephalanthae Yunck., Mem. Torrey Bot. Club18: 123. 1932.—Type: Cuscuta cephalanthi Engelm.

Lepidanche Engelm., Amer. J. Sci. Arts 43: 343, 1842. Cuscutasubsect. Lepidanche (Engelm.) Engelm, Trans. Acad. Sci.St. Louis 1(3): 509. 1859.—TYPE: Lepidanche compositarumEngelm. (= Cuscuta glomerata Choisy)

Inflorescences paniculiform to glomerulate or sometimesrope-like; numerous bracts similar to calyx lobes presentin some species at the base of the flowers (C. compacta,C. cuspidata, C. glomerata, C. squamata). Flowers 2–6 mm;calyx campanulate, 1/2 to equaling corolla tube, divided1/2–2/3 (or nearly to the base in the sp. with multiplebracts); lobes obtuse to acute; corolla campanulate to cylin-drical, lobes obtuse to acute straight; infrastaminal scales1/2 to equaling corolla tube, with very long fimbriae;pollen grains 3(4)-colpate, tectum imperforate or perfo-rate; styles cylindrical, thin; stigmas globose, small. Fruitindehiscent, globose (depressed-globose in C. cephalanthi),commonly narrowed/thickened distally. Figures 4L–M.


Note—Yuncker (1932) limited subsect. Oxycarpae ofEngelmann (1859) to include only C. gronovii, C. rostrata, andC. umbrosa. Our phylogenetic results (Stefanovic et al. 2007;Garcıa et al. 2014) also placed in this group several specieswith multiple bracts (C. compacta, C. cuspidata, C. squamata,and C. glomerata), which were initially considered to form adistinct genus, Lepidanche (Engelmann 1842), and later a sub-section of section Cleistogrammica (Engelmann 1859; Yuncker1932). In addition, C. cephalanthi, thought by Yuncker (1932)to form a monotypic subsection (Cephalanthae), is an integralpart of this group.

Included Species—Section Oxycarpae includes eight spe-cies: C. cephalanthi Engelm., C. compacta Juss., C. cuspidataEngelm., C. glomerata Choisy, C. gronovii Willd., C. rostrataShuttlew. ex Engelm. & A. Gray, C. squamata Engelm., andC. umbrosa Beyr. ex Hook.

Distribution—The group is North American; C. gronoviivar. gronovii was also introduced but not naturalised in WestIndies and West Europe.

15. Cuscuta sect. Racemosae (Yunck.) Costea & Stefanovic,stat. nov. Cuscuta subsect. Racemosae Yunck., Mem.Torrey Bot. Club 18: 143. 1932.—TYPE: Cuscuta racemosaMart.

Cuscuta subsect. Subinclusae Yunck., Mem. Torrey Bot. Club18: 166. 1932, in part (C. micranthaChoisy).—TYPE: Cuscutasubinclusa Dur. & Hilg.

Cuscuta subsect. Tinctoriae Yunck., Mem. Torrey Bot. Club18: 208. 1932, in part (only C. corniculata Engelm. andC. incurvata Prog.).—TYPE: Cuscuta tinctoriaMart.

Cuscuta subsect. Acutilobae Yunck., Mem. Torrey Bot. Club 18:201. 1932, in part (only C. xanthochortos Mart.).—TYPE:Cuscuta acutiloba Engelm.

Cuscuta subsect. Acutae Yunck., Mem. Torrey Bot. Club 18:152. 1932, in part (only C. globosa Ridl.).—TYPE: Cuscutaacuta Engelm.

Inflorescences paniculiform, corymbiform or fasciculate.Flowers 1.5–4 mm long; calyx campanulate to cylindrical, 1/2 to equaling corolla tube, divided 1/2–3/4, lobes acute orobtuse/rounded; corolla campanulate to cylindrical, lobesacute to obtuse; infrastaminal scales equalling corolla tube;pollen grains 3(4)-colpate, tectum imperforate or perforate;styles cylindrical, thin; stigmas globose, small. Fruit globose,indehiscent, commonly narrowed or thickened apically.Figures 4N–O.

Note—New additions to subsect. Racemosae of Yuncker(1932) based on molecular results (Stefanovic et al. 2007;Garcıa et al. 2014) are: C. micrantha (subsect. Subinclusae,Yuncker 1932), C. corniculata, C. incurvata (subsect. Tinctoriae,Yuncker 1932), C. globosa, and C. werdermannii (the latterincluded in subsect. Acutae by Hunziker 1949).

Included Species—Section Racemosae comprises 15 species:C. andina Phil.*, C. corniculata Engelm., C. globosa Ridl.*,C. incurvata Prog., C. micrantha Choisy, C. parviflora Engelm.,C. pauciflora Phil.*, C. peruviana Yunck.*, C. platyloba Prog.,C. racemosa Mart., C. suaveolens Ser., C. taimensis Ferreira &Dettke*, C. werdermannii Hunz., C. xanthochortos Mart. exEngelm., and C. yunckeriana Hunz.*

Distribution—All the species of sect. Racemosae are SouthAmerican. Cuscuta suaveolens was introduced at the endof the 19th century in North America, Europe, Africa, and

Australia with seeds of alfalfa but it did not naturalize onthese continents.

16. Cuscuta sect. Partitae Costea & Stefanovic, sect. nov.—TYPE: Cuscuta partita Choisy

Inflorescences corymbiform or paniculiform. Flowers 2–5 mm long; calyx campanulate, equalling to exceedingcorolla tube, divided almost to the base, lobes linear tolanceolate acute; corolla globose to campanulate; lobes linearto lanceolate, entire; infrastaminal scales equaling or exceed-ing corolla tube; pollen grains 3(4)-colpate, tectum imperfo-rate or perforate; styles cylindrical, thin; stigmas globose,small. Fruit dehiscent or indehiscent, globose or globose-depressed. Figures 4P–R.Note—Cuscuta partita and C. haughtii were thought by

Yuncker (1932) to belong to subsections Odontolepisae andAcutae, respectively. Cuscuta burrelllii and C. longiloba areamong the last species Cuscuta described by Yuncker (1957,1961), and the author was undecided about their placementeither in subsection Odontolepisae or Acutae.Included Species—Section Partitae includes five species:

C. burrellii Yunck., C. longiloba Yunck., C. haughtii Yunck.,C. partita Choisy, C. rojasii Hunz.*Distribution—Section Partitae is South American.

17. Cuscuta sect. Denticulatae (Yunck.) Costea & Stefanovic,stat. nov. Cuscuta subsect. Denticulatae Yunck., Mem.Torrey Bot. Club 18: 170. 1932, in part (all spp. exceptC. microstyla Engelm.).—TYPE: Cuscuta denticulata Engelm.

Cuscuta subsect. Subinclusae Yunck., Mem. Torrey Bot. Club18: 165. 1932, in part (only C. salina var. apoda (Yunck.)Yunck. = C. nevadensis I. M. Johnst.).—TYPE: Cuscutasubinclusa Dur. & Hilg.

Inflorescences glomerulate to umbelliform. Flowers 2–3 mm long; calyx cylindric-campanulate, ca. equalling corollatube, divided ca. 2/3 the length, lobes rounded to acute;corolla campanulate, lobes rounded to acute; infrastaminalscales equalling corolla tube; pollen grains 3(4)-colpate, tec-tum imperforate; styles cylindrical, thin; stigmas globose,small. Fruit indehiscent, globose-ovoid to ovoid, 1-seeded;embryo spherically enlarged. Figures 4S–T.Note—Yuncker (1932) placed in this group C. denticulata,

C. veatchii, and a South American species, C. microstyla(Yuncker 1932); however, the latter belongs to Sect. Subulatae(Stefanovic et al. 2007; Garcıa et al. 2014).Included Species—Section Denticulatae has three spe-

cies: C. denticulata Engelm., C. nevadensis I. M. Johnst., andC. veatchii Brandegee.Distribution—Cuscuta denticulata and C. nevadensis are

distributed in Western U. S. A. while C. veatchii grows is theCentral Desert of Baja California, Mexico.

18. Cuscuta sect. Lobostigmae Engelm. [“Lobostigma”], Trans.Acad. Sci. St. Louis 1: 512. 1859. Cuscuta subsect. Lobostigmae(Engelm.) Yunck., Mem. Torrey Bot. Club 18: 142. 1932.—TYPE: Cuscuta tasmanica Engelm., here designated.

Cuscuta subsect. Tinctoriae Yunck., Mem. Torrey Bot. Club 18:208. 1932, in part (only C. tinctoria Mart.).—TYPE:Cuscuta tinctoriaMart.

Cuscuta subsect. Subulatae Engelm. ex Yunck., Mem. TorreyBot. Club 18: 195. 1932, in part (only C. jalapensis)—TYPE: Cuscuta grandiflora Kunth.


Cuscuta subsect. Americanae Yunck., Mem. Torrey Bot. Club18: 217. 1932, in part (only C. floribunda Kunth).—TYPE:Cuscuta americana L.

Cuscuta subsect. Odontolepisae Yunck., Mem. Torrey Bot. Club18: 226. 1932, in part (only C. purpusii Yunck.).—TYPE:Cuscuta odontolepis Engelm.

Cuscuta subsect. Platycarpae Engelm. ex Yunck., Mem. TorreyBot. Club 18: 124. 1932, in part (only C. victorianaYunck.).—TYPE: C. obtusiflora Kunth

Inflorescences glomerulate to corymbiform. Flowers com-monly large and thick, 4–9 mm long (1.5–2.5 mm in C. victo-riana); Calyx campanulate to globose, 1/2 to equalling corollatube, divided 1/2–1/4 the length, lobes acute to rounded;corolla campanulate to globose, lobes acute to rounded;infrastaminal scales equalling corolla tube; pollen grains 3(4)-colpate, tectum imperforate, perforate, or microreticulate;styles cylindrical or subulate, thick (0.2–0.9 mm in diameter),stigmas large (0.25–0.6 mm in diameter), usually lobed. Fruitdehiscent (indehiscent in C. tasmaniana and C. victoriana).Figures 4V–W.Note—Both Engelmann (1859) and Yuncker (1932)

included in the section/subsection Lobostigmae onlyC. tasmanica. Phylogenetic results showed that C. tasmanicais a part of the second largest infrageneric group ofsubg. Grammica (Costea et al. 2013). Most of these species(C. jalapensis, C. mitriformis, C. rugosiceps, C. lindsayi andC. woodsonii) were placed by Yuncker (1932) in subsect.Subulatae, while others were originally included in othersubsections: Tinctoriae (C. tinctoria vars. tinctoria and aurea),Odontolepisae (C. purpusii), Americanae (C. tinctoria var.floribunda), and Platycarpae (C. victoriana) (Fig. 1). In addition,seven new species from this clade were recently described(Costea et al. 2008b; Costea et al. 2013).Included Species—Section Lobostigmae includes 18 species:

C. cotijana Costea & I. Garcıa, C. durangana Yunck*, C. iguanellaCostea & I. Garcıa, C. insolita Costea & I. Garcıa, C. jalapensisSchltdl., C. lindsayi Wiggins, C. mitriformis Engelm. ex Hemsl.[“mitraeformis”], C. montana Costea & Stefanovic, C. purpusiiYunck., C. rugosiceps Yunck., C. tasmanica Engelm., C. tateiYunck.*, C. timida Costea & Stefanovic, C. tinctoria Mart. exEngelm., C. tolteca Costea & Stefanovic, C. victoriana Yunck.,C. volcanica Costea & I. Garcıa, and C. woodsonii Yunck.Distribution—Section Lobostigmae is distributed in Mexico

and the adjacent areas (Southern U. S. A. and CentralAmerica); as an exception, C. tasmanica, C. tatei, andC. victoriana have a disjunct distribution in Australia.

Acknowledgments. The authors thank the curators/directors of theover 100 herbaria (see Materials and Methods) that made available theirspecimens for study. We are also grateful to Tom Van Devender, IgnacioGarcıa Ruiz, and Eleazar Carranza for sending additional plant material.Two anonymous reviewers kindly provided comments that improved thequality of the article. This research was supported by NSERC of CanadaDiscovery grants to M. Costea (327013) and S. Stefanovic (326439).

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